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(Chest. 2005;128:1225-1232.)
© 2005 American College of Chest Physicians

Arm Exercise and Hyperinflation in Patients With COPD*

Effect of Arm Training

Francesco Gigliotti, MD; Claudia Coli, MD; Roberto Bianchi, MD; Michela Grazzini, MD; Loredana Stendardi, MD; Carla Castellani, RT and Giorgio Scano, MD, FCCP

* From Fondazione Don C. Gnocchi, IRCCS, Pozzolatico, Florence, Italy.

Correspondence to: Giorgio Scano, MD, Section of Pulmonary Rehabilitation, Fondazione Don C. Gnocchi IRCCS, Via Imprunetana 124, 50020 Pozzolatico, Firenze, Italy; e-mail: uopneumo.pozzolatico{at}dongnocchi.it


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: Unlike studies on leg exercise, reports on the regulation of dynamic hyperinflation during arm exercise are scanty. We ascertained the following in patients with COPD: (1) whether and to what extent upper-limb exercise results in dynamic hyperinflation, and (2) the mechanism whereby an arm-training program (ATP) reduces arm effort and dyspnea.

Patients: Twelve patients with moderate-to-severe COPD were tested during incremental, symptom-limited arm exercise after a nonintervention control period (pre-ATP) and after ATP.

Methods: Exercise testing (1-min increments of 5 W) was performed using an arm ergometer. Oxygen uptake (O2), carbon dioxide output, minute ventilation (E), tidal volume, and respiratory rate (RR) were measured continuously during the tests. Inspiratory capacity (IC), exercise dyspnea, and arm effort using a Borg scale were assessed at each step of exercise.

Results: Arm exercise resulted in a significant decrease in IC and significant positive relationships of IC with an increase in O2 and exercise dyspnea and arm effort. The results of ATP were as follows: (1) a significant increase in exercise capacity (p < 0.001); (2) no change in the relationships of exercise dyspnea and arm effort with E and IC, and of IC with O2; (3) at a standardized work rate, E, exercise dyspnea, and arm effort significantly decreased, while the decrease in IC was significantly less (p < 0.01) than before the ATP; the decrease in E was accomplished primarily by a decrease in RR; and (4) at standardized E, exercise dyspnea and arm effort decreased significantly.

Conclusions: Arm exercise results in the association of dynamic hyperinflation, exercise dyspnea, and arm effort in COPD patients. An ATP increases arm endurance, modulates dynamic hyperinflation, and reduces symptoms.

Key Words: arm training • COPD • dynamic hyperinflation • dyspnea


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The increase in ventilation during leg exercise is accomplished by dynamic hyperinflation, which helps minimize expiratory flow limitation1 but increases dyspnea in patients with COPD.23 Unlike studies on leg exercise, reports on regulation of dynamic hyperinflation during arm exercise are scanty: simple arm elevation is associated with a mild increase in functional residual capacity (FRC)4 or a decrease in inspiratory capacity (IC)5 in COPD patients with moderate-to-severe obstruction. In contrast, arm exercise results in premature termination of expiration and an increase in dynamic hyperinflation in flow-limited patients with cystic fibrosis.6

Pulmonary rehabilitation programs improve exercise capacity by reducing both dynamic hyperinflation and dyspnea in patients with COPD.78 An arm-training program (ATP) leads to reduction in ventilatory requirements for simple arm elevation and increases the exercise level.910 Ratings of perceived dyspnea and fatigue decreased significantly in one study11 but not in another,9 so that the mechanisms of their improvement, if any, remain to be defined in patients with COPD.

Like leg-training programs, the effect of an ATP on dyspnea and arm fatigue could be due to a decrease in ventilatory requirements for a given level of activity,12 a decrease in dynamic hyperinflation,8 and desensitization.78 The aims of this study were therefore to ascertain the following in patients with COPD: (1) whether and to what extent upper-limb exercise results in dynamic hyperinflation, and (2) the mechanism whereby an ATP reduces arm effort and dyspnea.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Subjects
We studied 12 consecutive patients with stable, moderate-to-severe COPD who were entering an outpatient pulmonary rehabilitation program. Patients satisfied the following criteria: (1) a long history of smoking and moderate-to-severe, chronic dyspnea (Medical Research Council grade 2 to 4); (2) clinically stable condition, with no exacerbation or hospital admission in the preceding 4 weeks; and (3) no other significant disease(s) potentially contributing to dyspnea. The patients were all motivated to participate in the program and did not currently smoke.

Functional Evaluation
Routine spirometry with the subjects in a seated position was performed as previously described.1314 FRC was measured by helium dilution technique. The normal values for lung volumes are those proposed by the European Respiratory Society.15 Before performing exercise, the ventilatory patterns were evaluated with subjects sitting comfortably in an armchair with a mass-flow sensor (max; Sensor Medics; Yorba Linda, CA). From the spirogram, we derived the tidal volume (VT), respiratory rate (RR), and minute ventilation (E) [VT x RR].

Arm Ergometry
All patients performed an incremental (5 W/min), symptom-limited arm exercise. A modified stationary ergometer (Monarch Instrument; Varberg, Sweden) was used to deliver precise workload adjustments. The ergometer was secured to a table at shoulder level with the subjects seated in a straight-back chair. Each patient was made familiar with the apparatus days before the test. Expired gas was analyzed for E, oxygen uptake (O2), carbon dioxide output (CO2) using breath-by-breath analysis (max System; SensorMedics). CO2 and O2 were expressed as standard temperature and pressure, dry, and as a percentage of the predicted maximum O2.16

The ventilatory equivalent for oxygen (E/O2) and ventilatory efficiency (E/CO2) were also calculated. For each run, changes in E, VT, and RR were continuously recorded.

There was a continuous monitoring of 12-lead ECG and oxygen saturation by pulse oximetry (NPB 290; Nellcor Puritan Bennett; Pleasanton, CA). BP was recorded at rest and every 2 min during exercise, and recovery to baseline levels. Subjects were asked to perform two IC maneuvers during the last 30 s of each workload for the measurement of end-expiratory lung volume (EELV). The use of IC maneuvers to determine EELV is based on the assumption that total lung capacity (TLC) does not change during exercise in patients with COPD.17 IC maneuvers at peak exercise are shown to be a reliable measure of change in EELV in patients with COPD.18

The perception of exercise dyspnea and arm effort was evaluated each minute during exercise. Patients described dyspnea as a sensation of labored or difficult breathing experienced during cranking. Subjects were asked to rank the overall sensation of exercise dyspnea and arm effort on a large Borg scale from 0 (none) to 10 (maximal).19 The subjects were instructed that 0 signified no sensation at all, and that 10 signified the most severe sensation that they had ever experienced.

ATP
Each patient attended a 6-week outpatient pulmonary rehabilitation program. The program included education, breathing retraining, leisure walking, and unsupported arm exercise and arm training with an arm ergometer. For the training on the arm ergometer, the workload corresponding to 80% of the peak work rate (WR) observed in the pretraining incremental exercise test was set as the training intensity. Patients were instructed to maintain this work level until they reached a symptom limit. Sessions were closely supervised by a rehabilitation therapist; during the session, heart rate (HR) and arterial oxygen saturation were monitored. Unsupported arm exercise consisted of the following: (1) repetitive bilateral shoulder abduction and extension holding a light hand weight (0.5 to 1.0 kg) in a rhythm synchronized with breathing for 2-min periods; and (2) threading a set of rings in a series of pegs placed at different heights while the arm is held above the horizontal. The study was approved by the Ethics Committee of the Institution, and informed consent was obtained from subjects.

Protocol
This is a single-center, two-period, controlled study in which subjects complete a 6-week nonintervention period before entering a 6-week pulmonary rehabilitation program involving regular exercise training. In an initial screening, subjects were tested for pulmonary function and gas exchange. They became familiar with exercise testing procedures and the various scales for rating symptom intensity, and completed an incremental, symptom-limited exercise test. Three experimental visits were held at 6-week intervals immediately before the control period, after the control period (pre-ATP visit), and after ATP. Therefore, the subjects acted as their own controls. All visits were conducted at the same time of day for each subject.

Data Analysis
To compare responses to an identical level of exercise before and after the rehabilitation program, we selected the highest WR tolerated by a given patient during pre-ATP test, (the standardized WR). To compare responses to an identical level of ventilation, we selected the highest E tolerated by a given patient during the pre-ATP test (the standardized E). Nonparametric ratings of exertional breathlessness were compared before and after intervention using the Wilcoxon test. All other measurements made before and after ATP were analyzed using the paired t test. Pearson correlation coefficients were used to test the strength of the association between measured variables. A value of p < 0.05 was considered significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Anthropometric and baseline function data of the 12 patients with moderate-to-severe airflow obstruction and hyperinflation, mild-to-moderate hypoxia, and mild carbon dioxide retention are shown in Table 1 . The data did not change during the study.


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  		Table 1. Anthropometric and Lung Function Data*

 
Incremental Exercise Performance
At peak arm exercise, E, CO2, O2, HR, exercise dyspnea, arm effort, and WR all increased. The ATP did not modify E, CO2, O2, HR, exercise dyspnea, and arm effort but increased WR (p < 0.001) [Table 2 ]. The relationships of changes in exercise dyspnea and arm effort with changes in E, O2, CO2, and the relationships of changes in E with changes in O2 and CO2 were not altered with the ATP (Table 3 ).


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  		Table 2. Peak Exercise Response Before and After Rehabilitation*

 

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  		Table 3. Slopes of the Relationships of Changes in Exertional Dyspnea, Arm Effort, and E with changes in O2 and VCO2*

 
Changes at Standardized WR
With arm exercise, IC decreased by 0.93 ± 0.4 L (from 2.68 ± 0.79 to 1.75 ± 0.63 L, p < 0.000004) [mean ± SD]. After the ATP, IC decreased by 0.59 ± 0.27 L (from 2.6 ± 0.83 to 2.01 ± 0.81 L, p < 0.0001) and was significantly less (p < 0.01) than before ATP (Table 4 ). ATP lowered HR (p < 0.03) and decreased E (p < 0.01) by lengthening RR (p < 0.03) but did not modify O2 and CO2 (Table 5 ). Figure 1 (left panel) shows individual changes in both exercise dyspnea (average, from 5.6 ±1.3 to 3.6 ± 1.5 au; p < 0.02) and arm effort (average, from 6.5 ± 2.3 to 5.1 ± 2.3 arbitrary units [au]; p < 0.01) with the ATP. In most patients, exercise dyspnea and arm exercise decreased at standardized WR.


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  		Table 4. IC at Standardized WR (41.1 ± 13.6 W)

 

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  		Table 5. Exercise Response at Standardized WR (41.1 ± 13.6 W)*

 


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  		Figure 1. Changes in exercise dyspnea (ED) and arm exercise (AE) with an ATP at standardized WR (left panel) and standardized E (right panel).

 
Changes at Standardized E
The decrease in IC during arm exercise before ATP (0.68 ± 0.42 L; from 2.69 ± 0.62 to 2.01 ± 0.57 L; p < 0.03) tended to significantly differ (p < 0.057) from the decrease after ATP (0.43 ± 0.32 L; from 2.79 ± 0.66 to 2.35 ± 0.75 L; p < 0.007). ATP reduced exercise dyspnea (from 4 ± 1.7 to 2.75 ±1.2 au; p < 0.02) and arm effort (from 5.6 ± 3 to 4.6 ± 3.1 au; p < 0.01; Fig 1, right panel), lowered HR (p < 0.03), but did not modify WR, O2, CO2, VT, and RR (Table 6 ).


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  		Table 6. Exercise Response at Standardized E (37.3 ± 9.5 L/min)*

 
Relationships
Figure 2 shows the slopes of the relationships of changes in IC with changes in exercise dyspnea (left panel; all patients but patient 11) and arm effort (right panel; all patients but patients 6 and 11) before the ATP (r2 = 0.25 and r2 = 0.64, respectively) and after ATP (r2 = 0.37 and r2 = 0.60, respectively); no difference was found between before and after ATP. In each patient, a decrease in IC was significantly correlated with increase in O2 ({Delta}O2/{Delta}IC, 0.01 ± 0.03 L/min/L; from r = 0.73 to 0.96). This correlation did not significantly change after ATP ({Delta}O2/{Delta}IC, 0.009 ± 0.01 L/min/L; r = 0.67 to 0.98). Two representative subjects with the highest (patient 6, left panel) and the lowest (patient 7, right panel) response slopes of this relationship during arm exercise before and after ATP are shown in Figure 3 . The relationship between IC and O2 indicates that dynamic hyperinflation predicts a good amount of the variability in O2 during arm exercise.



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  		Figure 2. Left panel: Slopes of the relationships of changes in exercise dyspnea ({Delta}ED) with changes in IC ({Delta}IC) before and after ATP. Right panel: Slopes of the relationships of changes in arm exercise ({Delta}AE) with changes in IC before and after the ATP. Individual data points are shown. Bars are mean ± SD.

 


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  		Figure 3. Relationships of changes in IC with changes in O2 before and after the ATP in two representative subjects (patient 6, left panel; and patient 7, right panel). sl = slope.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Arm exercise resulted in dynamic hyperinflation, which directly correlated with increases in dyspnea, arm effort, and O2. The ATP resulted in the following: (1) a significant increase in exercise capacity at peak exercise; (2) a decrease in both ventilation and dynamic hyperinflation, primarily due to a decrease in RR at standardized WR; and (3) a decrease in dyspnea and arm effort at standardized WR and ventilation.

The novel finding of this study is the dynamic hyperinflation, ie, the increase in dynamic EELV during supported-arm exercise in patients with COPD. To the extent that TLC does not change appreciably during exercise in COPD,17 a change in IC accurately reflects the change in EELV.18 Dynamic hyperinflation minimizes expiratory flow limitation during lower-limb exercise in patients with severe COPD,238202122 but puts the respiratory muscles in a disadvantageous portion of their length/tension relationship and imposes an elastic load on the muscles during inspiration.23 Alison et al6 found that arm exercise may either increase EELV or reduce its decrease compared to leg exercise in healthy subjects, and diminish exercise capacity in flow-limited patients with cystic fibrosis. We explain dynamic hyperinflation with arm exercise in patients with COPD as being due to inadequate time to exhale the volume required to maintain EELV before the next inspiration begins.

Due to the load it places on an already stressed system, arm exercise contributes to dyspnea and disability in many patients with COPD.2324 In particular, the following are seen: (1) hyperinflation decreases maximal force-generating capacity of the respiratory muscle,2526 thereby increasing the central motor output to a weakened muscle; (2) the decrease in force-generating capacity increases the sense of inspiratory effort25; and (3) the association of an increased motor output with an increased respiratory system impedance increases the respiratory muscle load and may affect the coupling between inspiratory effort and concurrent inspiratory volume (neuromuscular dissociation of the ventilatory pump).23

Another finding of this study is the association between arm effort and dynamic hyperinflation. The rib cage and abdominal wall must be fixed to maintain the position of the torso during upper-limb exercise.27 This may result in a stiffer rib cage and the need for maintaining a particular ventilation by increasing the RR, and thereby dynamic hyperinflation, while the central output to the exercising arms increases.

Last but not least, the increase in dynamic hyperinflation predicted an average 69% of the variability in O2 (from 36 to 92%; Fig 3). These data confirm the results by Diaz et al28 during incremental, symptom-limited exercise on a cycle ergometer in stable patients with COPD. In that study, resting IC (IC percentage of predicted) explained 56% of the variance in maximum O2. Our data extend those results, in that dynamic hyperinflation during exercise largely predicts O2. Factors other than mechanical factors, such as deconditioning, are likely to explain the residual variance in O2. The present data also show that, regardless of leg or arm cycling, dynamic hyperinflation is a predictor of exercise tolerance in patients with COPD.28

Training that includes both upper- and lower-limb exercise may improve upper-extremity exercise endurance791011 and ratings of dyspnea.711 The effects of the ATP on dyspnea reduction must, however, be defined. Although respiratory function has generally been reported not to change after pulmonary rehabilitation programs, a mild decrease in FRC after upper-extremity exercise training has been found in patients with COPD.11 Ries et al11 showed, however, significant bronchodilator responsiveness at baseline, which may account for some of this improvement during training period.

Previous studies2930 of inhaled bronchodilator therapy in patients with COPD have shown that even a moderate reduction in dynamic hyperinflation may contribute to an improvement in dyspnea. Likewise, we have shown that rehabilitation programs based on leg exercise training decrease dynamic hyperinflation and reduce dyspnea.8 The present data clearly show the association between decreases in dynamic hyperinflation, RR, dyspnea, and arm effort at standardized WR. We explain the decrease in dynamic hyperinflation as being due to the increased time to exhale the volume required to maintain EELV before the next inspiration begins.

We found a significant relationship between IC and dyspnea and arm effort ratings during arm exercise (Fig 2), with the correlation coefficients being, however, as low as that found during leg exercise.8 These data suggest that, although dynamic hyperinflation contributes to exertional dyspnea in patients with COPD, additional physiologic and/or sensory factors are also important to the perception of dyspnea and arm effort during exercise. The reasons are as follows: (1) unlike the lack of changes in the slopes of ventilation with both O2 and CO2 (Table 3), ventilation decreased at standardized WR (Table 4); (2) changes in ventilation explained a consistent amount of changes in both dyspnea and arm effort before (r2 = 0.62 and r2 = 0.64, respectively) and after the ATP (r2 = 0.44 and r2 = 0.60, respectively); and (3) tolerance or desensitization to dyspnea and arm effort may allow patients to perform higher levels of work with reduced symptoms.73132 And indeed, at standardized ventilation, both arm effort and dyspnea were lower after the ATP as compared to before (Table 6). These findings indicate that both mechanical constraints and desensitization contribute to arm exercise-induced dyspnea after the training program. Furthermore, breathing retraining may have actually improved the breathing pattern, slowing the RR.33

A variable percentage of COPD patients stop leg exercise because of both dyspnea and leg effort, while others mostly stop because of either one or the other.7834 The present results showing in each subject a similar amount (increase and decrease) of both dyspnea and arm effort are consistent with the neural motor output being balanced between respiratory muscles, and arm and torso muscles.

Even though the small series of patients in this study should prevent us from drawing definite conclusions, our data indicate that arm exercise may result in the association of dynamic hyperinflation, dyspnea, and arm effort in patients with COPD. The ATP increases arm endurance, modulates dynamic hyperinflation, and reduces symptoms.


   Footnotes
 
Abbreviations: ATP = arm-training program; au = arbitrary unit; EELV = end-expiratory lung volume; FRC = functional residual capacity; HR = heart rate; IC = inspiratory capacity; RR = respiratory rate; TLC = total lung capacity; CO2 = carbon dioxide output; E = minute ventilation; O2 = oxygen uptake; VT = tidal volume; WR = work rate

This work was supported by a grant from the Fondazione Don C. Gnocchi ONLUS (IRCCS), Florence, Italy.

Received for publication July 23, 2004. Accepted for publication February 3, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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